University of South Florida Scholar Commons Graduate Theses and Dissertations Graduate School January 2012 Multisensory Integration in Shark Feeding Behavior Jayne M. Gardiner University of South Florida, [email protected] Follow this and additional works at: http://scholarcommons.usf.edu/etd Part of the American Studies Commons, Other Education Commons, Physiology Commons, and the Social and Behavioral Sciences Commons Scholar Commons Citation Gardiner, Jayne M., "Multisensory Integration in Shark Feeding Behavior" (2012). Graduate Theses and Dissertations. http://scholarcommons.usf.edu/etd/4046 This Dissertation is brought to you for free and open access by the Graduate School at Scholar Commons. It has been accepted for inclusion in Graduate Theses and Dissertations by an authorized administrator of Scholar Commons. For more information, please contact [email protected]. Multisensory Integration in Shark Feeding Behavior by Jayne Michelle Gardiner A dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy Department of Integrative Biology College of Arts and Sciences University of South Florida Co-Major Professor: Philip J. Motta, Ph.D. Co-Major Professor: Robert E. Hueter, Ph.D. Jelle Atema, Ph.D. Stephen M. Deban, Ph.D. Lynn B. Martin, Ph.D. Date of Approval: December 8, 2011 Keywords: olfaction, lateral line, electroreception, vision Copyright © 2012, Jayne Michelle Gardiner DEDICATION “It’s a wonderful thing to get an education” – Eugene C. Everett This work is dedicated to the memory of my grandfathers, Paul F. Gardiner (1920 – 2010), the great outdoorsman, who inspired my love of nature, and Eugene C. Everett (1928 – 2009), who nurtured my childhood fascination with aquatic animals and whose final words to me gave me the strength and courage to persevere, even when this goal seemed unattainable. I owe this accomplishment to their constant love, support, and encouragement. ACKNOWLEDGEMENTS This study represents a massive undertaking and assistance was provided by an incredible number of people, some of whom will inevitably be forgotten here, but whose contributions are nevertheless greatly appreciated. I would first like to acknowledge and thank my advisory team: my co-major advisors, Drs. Phil Motta and Bob Hueter for their guidance, encouragement, and support, and Dr. Jelle Atema, who opened the door to graduate work by taking a chance on a Microbiology and Immunology student who wanted to study fish. Thank you also to my committee members, Drs. Stephen Deban and Lynn Martin for their guidance, and to Dr. Jason Rohr for advice on the statistical analyses. I am forever indebted to Jack Morris, who designed, built, and maintained the flume system, collected and maintained animals, helped troubleshoot equipment and procedures, and somehow tolerated my many mistakes along the way. Logistical assistance with much of the above was also provided by Mercedes Smith. Thank you to Henry Luciano for troubleshooting the numerous computer and camera issues, even late night and on holidays, and to Karen Taylor for providing computer equipment. My assistants, Mote volunteer Rachel Dryer and USF REU intern Brittany Leigh, contributed greatly to the analysis of all of the video files. Assistance with animal collections and transportation were provided by Rhys Probyn, Ed Enos, Bill Klimm, Nate Goddard, Bryant Turffs, Pete Hull, Dean Dougherty, Greg Byrd, numerous Mote interns and volunteers. Assistance with animal care, husbandry and animal health issues were provided by Dr. Roxanna Smolowitz, Dr. Andy Stamper, Lynne Bird, and Matt Seguin. Advice on the design of the project, technical help, and loans of equipment were provided by Dr. Brandon Casper, Dr. David Mann, Dr. Stephen Kajiura, Clint Steffan, and Joe Gaspard. The use of microscope equipment and technical advice were provided by Dr. Gary Litman, Dr. Donna Eason, Diana Skapura, Tony Greco, Louis Kerr, and Dr. Jackie Webb. Years of helpful discussions, brainstorming, advice, logistical help, and comic relief were provided by my USF labmates, Kyle Mara, Samantha Mulvany, Lisa Whitenack, Laura Habegger, and Janne Pfeiffenberger, and my Mote Center for Shark Research colleagues, Dr. Carl Luer, Dr. Cathy Walsh, Dr. Nick Whitney, Dr. Jennifer Yordy, Dr. Jose Castro, Stephanie Leggett, and Jodi Miedema. This project was an inter- disciplinary and inter-institutional collaboration, with work conducted at the Marine Biological Laboratory in Woods Hole, MA and Mote Marine Laboratory in Sarasota, FL. I would like to thank everyone at both institutions for making me feel welcome, particularly Erin Kinney Dikmanis and Andris Dikmanis, who put a roof over my head on Cape Cod. Finally, thank you to all of my friends and family, particularly my parents, Michael and Betty Gardiner, for always believing in me and encouraging me when the going got tough, I couldn’t have done it without you. Funding for this work was provided by the National Science Foundation (IOS-083440, IOS-0841502, and IOS- 0841478), a Nelson Behavior Award from the American Elasmobranch Society, a Raney Fund Award from the American Society of Ichthyologists and Herpetologists, a Lerner- Gray Grant for Marine Research from the American Museum of Natural History, and the Porter Family Foundation. TABLE OF CONTENTS List of Tables ..................................................................................................................... iv List of Figures ......................................................................................................................v Abstract ............................................................................................................................ viii Chapter One. The Sensory Biology of Sharks .....................................................................1 Introduction ..............................................................................................................1 Chemoreception .......................................................................................................2 Olfaction ......................................................................................................3 Gustation ......................................................................................................8 Solitary Chemosensory Cells .......................................................................9 The Common Chemical Sense ...................................................................10 Hearing ...................................................................................................................10 Mechanoreception ..................................................................................................12 Vision .....................................................................................................................16 Electroreception .....................................................................................................22 Multimodal Integration ..........................................................................................25 Experimental Animals ...........................................................................................29 The Smooth Dogfish, Mustelus canis ........................................................29 The Nurse Shark, Ginglymostoma cirratum ..............................................29 The Bonnethead, Sphyrna tiburo ...............................................................30 The Blacktip Shark, Carcharhinus limbatus .............................................31 Literature Cited ......................................................................................................32 Chapter Two. The Function of Bilateral Odor Arrival Time Differences in Olfactory Orientation of Sharks .............................................................................68 Summary ....................................................................................................68 Results and Discussion ..............................................................................69 Experimental Procedures ...........................................................................76 Supplemental Information .........................................................................79 Supplemental Data .........................................................................79 Supplemental Experimental Procedures ........................................80 Experimental Animals .......................................................80 Headstage Apparatus .........................................................81 Odor Stimuli.......................................................................82 Literature Cited ..........................................................................................83 i Chapter Three. Multisensory Integration in Food Search Behaviors ................................89 Abstract ..................................................................................................................89 Introduction ............................................................................................................90 Materials and Methods ...........................................................................................97 Experimental Animals ...............................................................................97 Behavioral Procedures ...............................................................................98 Sensory